Protein quality in bacterial inclusion bodies

Recombinant protein folding and misfolding in Escherichia coli

Baneyx, F., & Mujacic, M. (2004) · Nature Biotechnology · doi:10.1038/nbt1029 · Cited by 1,445

Protein aggregation: folding aggregates, inclusion bodies and amyloid

Fink, A. L. (1998) · Folding and Design · doi:10.1016/s1359-0278(98)00002-9 · Cited by 1,157

Amyloid fibrillogenesis: themes and variations

Rochet, J.-C., & Lansbury, P. T. (2000) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(99)00049-4 · Cited by 1,095

Rationalization of the effects of mutations on peptide andprotein aggregation rates

Chiti, F., Stefani, M., Taddei, N., Ramponi, G., & Dobson, C. M. (2003) · Nature · doi:10.1038/nature01891 · Cited by 1,072

Advanced genetic strategies for recombinant protein expression in Escherichia coli

Sørensen, H. P., & Mortensen, K. K. (2005) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2004.08.004 · Cited by 963

Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli

Sørensen, H. P., & Mortensen, K. K. (2005) · Microbial Cell Factories · doi:10.1186/1475-2859-4-1 · Cited by 841

The power of two: protein dimerization in biology

Marianayagam, N. J., Sunde, M., & Matthews, J. M. (2004) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2004.09.006 · Cited by 599

Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB

Mogk, A. (1999) · The EMBO Journal · doi:10.1093/emboj/18.24.6934 · Cited by 595

Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network

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Protein refolding for industrial processes

Clark, E. D. B. (2001) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(00)00200-7 · Cited by 507

Advances in refolding of proteins produced in E. coli

Lilie, H., Schwarz, E., & Rudolph, R. (1998) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(98)80035-9 · Cited by 476

Thermotolerance Requires Refolding of Aggregated Proteins by Substrate Translocation through the Central Pore of ClpB

Weibezahn, J., Tessarz, P., Schlieker, C., Zahn, R., Maglica, Z., Lee, S., Zentgraf, H., Weber-Ban, E. U., Dougan, D. A., Tsai, F. T. F., et al. (2004) · Cell · doi:10.1016/j.cell.2004.11.027 · Cited by 459

Practical considerations in refolding proteins from inclusion bodies

Tsumoto, K., Ejima, D., Kumagai, I., & Arakawa, T. (2003) · Protein Expression and Purification · doi:10.1016/s1046-5928(02)00641-1 · Cited by 452

Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation

Mogk, A., Deuerling, E., Vorderwülbecke, S., Vierling, E., & Bukau, B. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03710.x · Cited by 374

Preparative protein refolding

Middelberg, A. P. J. (2002) · Trends in Biotechnology · doi:10.1016/s0167-7799(02)02047-4 · Cited by 370

Protein aggregation in recombinant bacteria: biological role of inclusion bodies

Villaverde, A., & Mar Carrió, M. (2003) · Biotechnology Letters · doi:10.1023/a:1025024104862 · Cited by 345

Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins

García-Fruitós, E., González-Montalbán, N., Morell, M., Vera, A., Ferraz, R. M., Arís, A., Ventura, S., & Villaverde, A. (2005) · Microbial Cell Factories · doi:10.1186/1475-2859-4-27 · Cited by 319

Specific aggregation of partially folded polypeptide chains: The molecular basis of inclusion body composition

Speed, M. A., Wang, D. I. C., & King, J. (1996) · Nature Biotechnology · doi:10.1038/nbt1096-1283 · Cited by 312

Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins

Vallejo, L. F., & Rinas, U. (2004) · Microbial Cell Factories · doi:10.1186/1475-2859-3-11 · Cited by 311

Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli

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Refolding of Substrates Bound to Small Hsps Relies on a Disaggregation Reaction Mediated Most Efficiently by ClpB/DnaK

Mogk, A., Schlieker, C., Friedrich, K. L., Schönfeld, H.-J., Vierling, E., & Bukau, B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303587200 · Cited by 279

Heat-inactivated proteins are rescued by the DnaK⋅J-GrpE set and ClpB chaperones

Motohashi, K., Watanabe, Y., Yohda, M., & Yoshida, M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.13.7184 · Cited by 251

Amyloid-like Properties of Bacterial Inclusion Bodies

Carrió, M., González-Montalbán, N., Vera, A., Villaverde, A., & Ventura, S. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.02.030 · Cited by 249

Disrupting the hydrophobic patches at the antibody variable/constant domain interface: improved in vivo folding and physical characterization of an engineered scFv fragment

Nieba, L., Honegger, A., Krebber, C., & Pluckthun, A. (1997) · Protein Engineering Design and Selection · doi:10.1093/protein/10.4.435 · Cited by 248

Molecular chaperones, folding catalysts, and the recovery of active recombinant proteins fromE. coli: To fold or to refold

Thomas, J. G., Ayling, A., & Baneyx, F. (1997) · Applied Biochemistry and Biotechnology · doi:10.1007/bf02785589 · Cited by 244

Short amino acid stretches can mediate amyloid formation in globular proteins: The Src homology 3 (SH3) case

Ventura, S., Zurdo, J., Narayanan, S., Parreño, M., Mangues, R., Reif, B., Chiti, F., Giannoni, E., Dobson, C. M., Aviles, F. X., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308249101 · Cited by 241

Roles of Individual Domains and Conserved Motifs of the AAA+ Chaperone ClpB in Oligomerization, ATP Hydrolysis, and Chaperone Activity

Mogk, A., Schlieker, C., Strub, C., Rist, W., Weibezahn, J., & Bukau, B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209686200 · Cited by 239

Inclusion Bodies: Formation and Utilisation

Fahnert, B., Lilie, H., & Neubauer, P. (2004) · Advances in Biochemical Engineering/Biotechnology · doi:10.1007/b93995 · Cited by 226

Construction and deconstruction of bacterial inclusion bodies

Carrió, M. M., & Villaverde, A. (2002) · Journal of Biotechnology · doi:10.1016/s0168-1656(02)00032-9 · Cited by 224

Substrate recognition by the AAA+ chaperone ClpB

Schlieker, C., Weibezahn, J., Patzelt, H., Tessarz, P., Strub, C., Zeth, K., Erbse, A., Schneider-Mergener, J., Chin, J. W., Schultz, P. G., et al. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb787 · Cited by 223

Protein Misfolding and Inclusion Body Formation in Recombinant Escherichia coli Cells Overexpressing Heat-shock Proteins

Thomas, J. G., & Baneyx, F. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.19.11141 · Cited by 223

An amyloid-forming segment of β2-microglobulin suggests a molecular model for the fibril

Ivanova, M. I., Sawaya, M. R., Gingery, M., Attinger, A., & Eisenberg, D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403756101 · Cited by 219

Prediction of "hot spots" of aggregation in disease-linked polypeptides

de Groot, N. S., Pallarés, I., Avilés, F. X., Vendrell, J., & Ventura, S. (2005) · BMC Structural Biology · doi:10.1186/1472-6807-5-18 · Cited by 204

Native-like Secondary Structure in Interleukin-1.beta. Inclusion Bodies by Attenuated Total Reflectance FTIR

Oberg, K., Chrunyk, B. A., Wetzel, R., & Fink, A. L. (1994) · Biochemistry · doi:10.1021/bi00175a035 · Cited by 202

Renaturation of Escherichia coli Tryptophanase after Exposure to 8 M Urea: Evidence for the Existence of Nucleation Centers

LONDON, J., SKRZYNIA, C., & GOLDBERG, M. E. (1974) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1974.tb03707.x · Cited by 197

In vitro protein refolding by chromatographic procedures

Li, M., Su, Z.-G., & Janson, J.-C. (2004) · Protein Expression and Purification · doi:10.1016/j.pep.2003.08.023 · Cited by 191

Factors influencing inclusion body formation in the production of a fused protein in Escherichia coli

Strandberg, L., & Enfors, S. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.6.1669-1674.1991 · Cited by 185

Understanding the relationship between the primary structure of proteins and its propensity to be soluble on overexpression in Escherichia coli

Idicula‐Thomas, S., & Balaji, P. V. (2005) · Protein Science · doi:10.1110/ps.041009005 · Cited by 175

Production of Nonclassical Inclusion Bodies from Which Correctly Folded Protein Can Be Extracted

Jevševar, S., Gaberc-Porekar, V., Fonda, I., Podobnik, B., Grdadolnik, J., & Menart, V. (2008) · Biotechnology Progress · doi:10.1021/bp0497839 · Cited by 175

Protein aggregation as bacterial inclusion bodies is reversible

Carrió, M. M., & Villaverde, A. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02073-7 · Cited by 167

Thermolabile folding intermediates: inclusion body precursors and chaperonin substrates

King, J., Haase‐Pettingell, C., Robinson, A. S., Speed, M. A., & Mitraki, A. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.1.8566549 · Cited by 150

Mining the Structural Genomics Pipeline: Identification of Protein Properties that Affect High-throughput Experimental Analysis

Goh, C.-S., Lan, N., Douglas, S. M., Wu, B., Echols, N., Smith, A. A., Milburn, D., Montelione, G. T., Zhao, H., & Gerstein, M. (2003) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.11.053 · Cited by 146

Substrate Shuttling Between the DnaK and GroEL Systems Indicates a Chaperone Network Promoting Protein Folding

Buchberger, A., Schröder, H., Hesterkamp, T., Schönfeld, H., & Bukau, B. (1996) · Journal of Molecular Biology · doi:10.1006/jmbi.1996.0465 · Cited by 145

Fine architecture of bacterial inclusion bodies

Carrió, M., Cubarsí, R., & Villaverde, A. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01357-0 · Cited by 144

Localization of Chaperones DnaK and GroEL in Bacterial Inclusion Bodies

Carrió, M., & Villaverde, A. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.10.3599-3601.2005 · Cited by 136

Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy

Ami, D., Natalello, A., Taylor, G., et al. (2006) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2005.12.005 · Cited by 134

Characterization of the aggregates formed during recombinant protein expression in bacteria

Schrödel, A., & de Marco, A. (2005) · BMC Biochemistry · doi:10.1186/1471-2091-6-10 · Cited by 131

Secondary structure characterization of ß-lactamase inclusion bodies

Przybycien, T. M., Dunn, J. P., Valax, P., & Georglou, G. (1994) · Protein Engineering Design and Selection · doi:10.1093/protein/7.1.131 · Cited by 129

Inclusion body formation and protein stability in sequence variants of interleukin-1 beta.

Chrunyk, B. A., Evans, J., Lillquist, J. S., Young, P. R., & Wetzel, R. B. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)46810-4 · Cited by 127

Bioprocessing of Therapeutic Proteins from the Inclusion Bodies of Escherichia coli

Panda, A. K. (2003) · Advances in biochemical engineering, biotechnology · doi:10.1007/3-540-36466-8_3 · Cited by 124

Protein expression and refolding – A practical guide to getting the most out of inclusion bodies

Cabrita, L. D., & Bottomley, S. (2004) · Biotechnology annual review · doi:10.1016/s1387-2656(04)10002-1 · Cited by 120

Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants

Kitagawa, M., 宮川, 瑞., Matsumura, Y., & Tsuchido, T. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.02958.x · Cited by 119

SPINE: an integrated tracking database and data mining approach for identifying feasible targets in high-throughput structural proteomics

Bertone, P. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.13.2884 · Cited by 118

Unscrambling an egg: protein disaggregation by AAA+ proteins

Weibezahn, J., Bukau, B., & Mogk, A. (2004) · Microbial Cell Factories · doi:10.1186/1475-2859-3-1 · Cited by 115

High activity of inclusion bodies formed in Escherichia coli overproducing Clostridium thermocellum endoglucanase D

Tokatlidis, K., Dhurjati, P., Millet, J., Béguin, P., & Aubert, J.-P. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)80478-l · Cited by 114

[3] Isolating inclusion bodies from bacteria

Georgiou, G., & Valax, P. (1999) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(99)09005-9 · Cited by 110

Novel insights into the mechanism of chaperone-assisted protein disaggregation

Weibezahn, J., Schlieker, C. D., Tessarz, P., Mogk, A., & Bukau, B. (2005) · Biological Chemistry · doi:10.1515/bc.2005.086 · Cited by 108

Role of molecular chaperones in inclusion body formation

Carrió, M., & Villaverde, A. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00126-1 · Cited by 108

Expression of Eukaryotic Proteins in Soluble Form inEscherichia coli

Zhang, Y., Olsen, D. R., Nguyen, K. B., Olson, P. S., Rhodes, E. T., & Mascarenhas, D. D. (1998) · Protein Expression and Purification · doi:10.1006/prep.1997.0834 · Cited by 106

High-Throughput Expression of C. elegans ProteinsPreprint

Luan, C.-H., Qiu, S., Finley, J. B., Carson, M., Gray, R. J., Huang, W., Johnson, D. H., Tsao, J., Reboul, J., Vaglio, P., et al. (2004) · Genome Research · doi:10.1101/gr.2520504 · Cited by 104

Protein quality control in the bacterial periplasm

Miot, M., & Betton, J. (2004) · Microbial Cell Factories · doi:10.1186/1475-2859-3-4 · Cited by 97

Kinetics of inclusion body formation studied in intact cells by FT‐IR spectroscopy

Ami, D., Natalello, A., Gatti‐Lafranconi, P., Lotti, M., & Doglia, S. M. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.04.085 · Cited by 96

Protein compositional analysis of inclusion bodies produced in recombinant Escherichia coli

Rinas, U., & Bailey, J. E. (1992) · Applied Microbiology and Biotechnology · doi:10.1007/bf00240735 · Cited by 87

Molecular Characterization of β‐Lactamase Inclusion Bodies Produced in Escherichia coli. 1. Composition

Valax, P., & Georgiou, G. N. (1993) · Biotechnology Progress · doi:10.1021/bp00023a014 · Cited by 84

Dynamics of in vivo protein aggregation: building inclusion bodies in recombinant bacteria

Carrio, M. M., Corchero, J. L., & Villaverde, A. (1998) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1998.tb13292.x · Cited by 81

The formation of biologically active beta-galactosidase inclusion bodies in Escherichia coli.

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Protein composition of Vitreoscilla hemoglobin inclusion bodies produced in Escherichia coli.

Hart, R. A., Rinas, U., & Bailey, J. E. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)38405-4 · Cited by 73

Molecular Chaperones: Structure of a Protein Disaggregase

Mogk, A., & Bukau, B. (2004) · Current Biology · doi:10.1016/j.cub.2003.12.051 · Cited by 71

FT-IR study of heterologous protein expression in recombinant Escherichia coli strains

Ami, D., Bonecchi, L., Calı̀, S., Orsini, G., Tonon, G., & Doglia, S. M. (2003) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2003.09.008 · Cited by 60

Mutations in Human Interferon Gamma Affecting Inclusion Body Formation Identified by a General Immunochemical Screen

Wetzel, R. B., Perry, L. J., & Veilleux, C. (1991) · Nature Biotechnology · doi:10.1038/nbt0891-731 · Cited by 60

Characterization of inclusion bodies in recombinant Escherichia coli producing high levels of porcine somatotropin

Rinas, U., Boone, T. C., & Bailey, J. E. (1993) · Journal of Biotechnology · doi:10.1016/0168-1656(93)90179-q · Cited by 46

Folding of a misfolding‐prone β‐galactosidase in absence of DnaK

García‐Fruitós, E., Carrió, M., Arı́s, A., & Villaverde, A. (2005) · Biotechnology and Bioengineering · doi:10.1002/bit.20496 · Cited by 35

Structural characteristics and refolding of in vivo aggregated hyperthermophilic archaeon proteins

Umetsu, M., Tsumoto, K., Kumar, A., Nitta, S., Tanaka, Y., Adschiri, T., & Kumagai, I. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)01441-8 · Cited by 34

Mutational effects on inclusion body formation in the periplasmic expression of the immunoglobulin VL domain REI

Chan, W., Helms, L. R., Brooks, I. S., Lee, G., Ngola, S. M., McNulty, D. E., Maleeff, B. E., Hensley, P., & Wetzel, R. B. (1996) · Folding and Design · doi:10.1016/s1359-0278(96)00017-x · Cited by 33

Improving solubility of catalytic domain of human β‐1,4‐galactosyltransferase 1 through rationally designed amino acid replacements

Malissard, M., & Berger, E. G. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02357.x · Cited by 29

How to find soluble proteins: a comprehensive analysis of alpha/beta hydrolases for recombinant expression in E. coli

Koschorreck, M., Fischer, M. J., Barth, S., & Pleiss, J. (2005) · BMC Genomics · doi:10.1186/1471-2164-6-49 · Cited by 28

Evidence that the methylesterase of bacterial chemotaxis may be a serine hydrolase

Krueger, J. K., Stock, J. B., & Schutt, C. E. (1992) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(92)90220-8 · Cited by 14

The CamSol method of rational design of protein mutants with enhanced solubility

Sormanni, P., Aprile, F. A., & Vendruscolo, M. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.09.026 · Cited by 494

Protein recovery from inclusion bodies of Escherichia coli using mild solubilization process

Singh, A., Upadhyay, V., Upadhyay, A. K., Singh, S. M., & Panda, A. K. (2015) · Microbial Cell Factories · doi:10.1186/s12934-015-0222-8 · Cited by 444

Bimodal protein solubility distribution revealed by an aggregation analysis of the entire ensemble of Escherichia coli proteins

Niwa, T., Ying, B.-W., Saito, K., Jin, W., Takada, S., Ueda, T., & Taguchi, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811922106 · Cited by 321

Kinetics of Inclusion Body Formation and Its Correlation with the Characteristics of Protein Aggregates in Escherichia coli

Upadhyay, A. K., Murmu, A., Singh, A., & Panda, A. K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033951 · Cited by 118

A relationship between mRNA expression levels and protein solubility in E. coli

Tartaglia, G. G., Pechmann, S., Dobson, C. M., & Vendruscolo, M. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.03.002 · Cited by 63